Infection (2019) 47:1059–1063 https://doi.org/10.1007/s15010-019-01344-z

CASE REPORT

Non‑typhoidal Salmonella aortitis

Giulia Gardini1 · Paola Zanotti1 · Alessandro Pucci2 · Lina Tomasoni1 · Silvio Caligaris1 · Barbara Paro2 · Emanuele Gavazzi3 · Domenico Albano4 · Stefano Bonardelli2 · Roberto Maroldi3 · Rafaele Giubbini4 · Francesco Castelli1

Received: 18 April 2019 / Accepted: 12 July 2019 / Published online: 18 July 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract Non-typhoidal Salmonella (NTS) spp. causes about 40% of all infective aortitis and it is characterized by high morbidity and mortality. Human infection occurs by fecal–oral transmission through ingestion of contaminated food, milk, or water (inter-human or zoonotic transmission). Approximately 5% of patients with NTS gastroenteritis develop bacteremia and the incidence of extra-intestinal focal infection in NTS bacteremia is about 40%. The organism can reach an extra-intestinal focus through blood dissemination, direct extension from the surrounding organs and direct bacterial inoculation (e.g. inva- sive medical procedures). Medical and surgical interventions are both needed to successfully control the infection. Here, we report a case of abdominal sub-renal aortitis caused by Salmonella enterica serovar Enteritidis in an 80-year-old man.

Keywords Salmonella · Aortitis · Extra-intestinal localization by Salmonella

Case report non-tender, painless abdomen with normal bowel sounds, no Murphy sign, negative costovertebral angle (CVA) ten- In October 2018, a 80-year-old man came to the Emergency derness test, normal pulmonary and cardiac sounds). Labo- Department of ASST Spedali Civili Hospital in Brescia ratory tests showed mild leukocytosis with prevalence of complaining of a 4 day history of fever (maximum tempera- neutrophils, mild normocytic anemia, increased C reactive ture 39 °C) and a single day of diarrhea (2–3 episodes). At protein (CRP 129 mg/mL, normal value < 5 mg/mL) and home, he had taken amoxicillin–clavulanate (1 gr bid) for erythrocyte sedimentation rate (ESR 62 mm/h, normal value 3 days without clinical beneft. His medical history was char- 3–46 mm/h), slight increase of transaminases, ALP (alkaline acterized by hypertension on medical treatment, diabetes phosphatase), and GGT (gamma-glutamyl transpeptidase). mellitus managed by diet, chronic ischemic heart disease, Chemical–physical examination of urine, chest X-ray and dyslipidemia on medical treatment, valved prosthesis of abdominal ultrasound were normal. the ascending aorta, widespread atherosclerosis and sigma He was admitted to the Department of Infectious and diverticulosis. Tropical Diseases, where empirical therapy with pipera- Clinically, he was feverish, hemodynamically stable and cillin–tazobactam plus amikacin was started, after col- with no evident focus of infection (no skin lesions, soft, lecting blood samples for culture. A pansensitive strain of Salmonella enterica serovar Enteritidis grew rapidly from blood culture and the ongoing antibiotic therapy remained * Giulia Gardini unchanged. Stool culture, performed under antibiotic ther- [email protected] apy because of constipation, was negative. Blood cultures 1 Department of Infectious and Tropical Diseases, ASST performed on hospital days 4 and 8 resulted negative. Spedali Civili and University of Brescia, Brescia, Italy The patient was asked about potential risk factors for Sal- 2 Department of Vascular Surgery, ASST Spedali Civili monella spp. infection. He lived alone in a rural area and and University of Brescia, Brescia, Italy he reported recent consumption of farmer’s eggs (3–4 days 3 Department of Radiology, ASST Spedali Civili, Brescia, before the onset of symptoms). He denied recent contacts Italy with animals or persons with fever or gastrointestinal symp- 4 Department of Nuclear Medicine, ASST Spedali Civili, toms, and no history of recent travel was reported. Brescia, Italy

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He complained of constipation from the beginning of decided to postpone an intervention until a better control of the hospital admission. After a few days, he complained the infection was reached, setting up a radiological weekly of severe widespread abdominal pain with slight positive control. From hospital days 4 to 11, some other radiological Blumberg sign (rebound tenderness) in the right hypogastric investigations were performed to exclude the involvement area and reduced peristalsis. Abdomen X-ray was performed of the heart and other parts of the aorta: thorax CT scan showing mild coprostasis, so that he was treated with laxa- with contrast and trans-esophageal echocardiography were tives with rapid clinical beneft. The day after he was again normal and fuorine-18-fuorodeoxyglucose (FDG) posi- feverish (maximum temperature 39 °C) and with severe per- tron emission tomography/computed tomography showed sistent abdominal and lumbar pain. An urgent angio-CT scan a pathological FDG uptake only in the sub-renal aortic wall was performed and sub-renal aortitis was diagnosed (see and in the surrounding fatty tissue (see Fig. 2). Fig. 1). Vascular surgeons urgently evaluated the patient and To exclude other major causes of aortitis, he was screened for syphilis (negative TPHA) and autoimmune diseases (nor- mal C3, C4, anti-nuclear antibodies, anti-neutrophylic cyto- plasmic antibodies and rheumatoid factor). We also checked conditions that predispose to NTS bac- teremia. He had no HIV infection, intestinal strongyloidia- sis, hemoglobinopathies, abnormal immunoglobulin dosage (except from a mild increased of IgA) nor abnormal lym- phocytic typing. During the second week of hospitalization, he showed an improvement of the temperature curve, a mild abdomi- nal pain under control of analgesic therapy, hemodynamic stability, symmetric and valid arterial pulses, improvement of infammation indices; angio-CT showed a slight increase of the aortic diameter (pseudoaneurysm) and the disappear- ance of the thrombus on the right side of the aortic wall. A week after, the patient became tachycardic, feverish (maxi- mum temperature 38.5 °C), with abdominal and lumbar pain that was no longer well controlled with medical therapy. Laboratory tests showed worsening anemia. A new angio- Fig. 1 Abdominal angio-CT scan performed on admission showed a CT scan was urgently performed, showing a further increase sub-renal pseudoaneurysm with irregular and enhancing thrombus, (more than 3 cm) of the pseudoaneurysm (see Fig. 3). He consistent with aortitis was urgently transferred to the Department of Vascular

Fig. 2 a Maximum intensity projection showing the presence of increased FDG uptake in the abdomen near the aorta. b Axial PET images. c Axial PET/CT fused images. d Coronal PET images. e Coronal PET/CT fused images confrming the hypermetabolic lesion in the right para-aortic tissue

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Fig. 3 Abdominal angio-CT scan performed 2 weeks after admission revealed an increas- ing sub-renal pseudoaneurysm without signifcant thrombosis

symptoms, presented normal infammatory indices, and the abdominal angio-CT was negative and showed no surgical complications (see Fig. 5). Therefore, antibiotic therapy was stopped after a total of 8 weeks (4 weeks of intravenous ther- apy and 4 weeks of oral therapy). Six months after the onset of his original symptoms, the patient was asymptomatic; he had no signs of relapse and his angio-CT scan remained negative.

Discussion

Fig. 4 Segment of the aorta from renal arteries to the carrefour Non-typhoidal Salmonella is a typical cause of aortitis char- replaced by a cryopreserved allograft acterized by high morbidity and mortality. Human infec- tion occurs by fecal–oral transmission through ingestion of Surgery and an open surgery was performed. After perform- contaminated food, milk, or water (inter-human or zoonotic ing a median laparotomy and opening retroperitoneum, a transmission). difuse lymphatic involvement of the periaortic tissue with It is mandatory to search for extra-intestinal foci of greater lymphadenopathies surrounding the pseudoaneurysm infection in patients with Salmonella spp. bacteremia, espe- and an aortic dissection from the supra-renal plane to the cially if the clinical and/or laboratory picture exhibits slow aortic bifurcation were revealed. The segment of the aorta improvement during appropriate antibiotic therapy or rapid from renal arteries (juxta-renal anastomosis) to the carre- worsening after interruption of antibiotics. In fact, the inci- four was replaced by a cryopreserved allograft (see Fig. 4). dence of extra-intestinal focal infection in NTS bacteremia A homograft patch was then positioned around the distal is high (about 40%) [1], and with regard to cardiovascular anastomosis as reinforcement. The homograft was fnally infection, it increases when there are predisposing conditions covered with a pedunculated omental fap fxed by multiple such as male gender, age over 50 years, hypertension, diabe- stitches to the retroperitoneum. tes, pathological alterations of the aortic wall (e.g. athero- After surgery, no post-operative complications were sclerosis), invasive catheterization or post-traumatic lesions, observed and the patient remained without fever with immunodefciency (e.g. HIV infection), solid-organ cancer, descending infammatory indices. Intravenous antibiotic atrial fbrillation, hemoglobinopathies, abnormal gastroin- therapy with piperacillin–tazobactam was never inter- testinal barrier and intestinal strongyloidiasis [1–10]. rupted, and about 4 weeks after admission, the patient Our patient did not report any risk factors for Salmo- was discharged with amoxicillin–clavulanate (1 gr qds). nella spp. infection, except for farmer’s eggs consump- About 4 weeks after discharge, he denied any pathological tion some days before. S. Enteritidis probably reached the

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Fig. 5 Abdominal angio-CT scan performed after surgery showed no signs of infection or complications

patient’s aorta through haematogenous spread after a pri- therapy [1, 3, 7–9]. Otherwise, prompt surgical intervention mary gastrointestinal infection. is necessary. In this patient, predisposing factors for NTS bactere- Optimal antibiotic duration is unclear. Some authors sug- mia and aortic infection included male gender, age over gest long-life suppressive therapy, whereas others suggest 50 years, hypertension, diabetes mellitus, widespread ath- antibiotic therapy lasting for at least 6–8 weeks with at least erosclerosis, and sigma diverticulosis. He had not HIV 3–4 weeks of intravenous therapy [1, 3, 7–9]. Essential fac- infection, hemoglobinopathies, intestinal strongyloidiasis, tors for choosing antibiotic duration are the possibility to abnormal immunoglobulin dosage nor abnormal lympho- associate a surgical intervention and the type of surgery used cytic typing. (open vs endovascular): we should consider long-life sup- To exclude other major causes of aortitis, he was screened pressive therapy in case of only medical management and for syphilis and autoimmune diseases with negative results. of endovascular treatment. Antibiotics alone are unsuccessful resulting in a mortal- Patients who have had aortic infection by Salmonella spp. ity of nearly 100% of cases, reduced to 40% with surgery have to be followed with clinical, blood, and radiological [1–5, 9]. Therefore, surgical treatment must always be con- examinations for years to be able to act rapidly in case of sidered. There are two options: endovascular treatment and complications or relapses after the completion of antibi- open surgery. The frst one has a lower early mortality rate, otic therapy [11, 12]. In this case, the patient was treated but late aneurysm-related events including mortality and with antibiotics for a total of 8 weeks, four of which intra- complications seem to be more common than conventional venously, planning a clinical and radiological long-term surgery, because the infected tissue cannot be removed. At follow-up. present, endovascular technique has consequently restricted indications: absence of gross purulence, gross infection, aorto-digestive fstula, uncontrolled sepsis and the presence Conclusion of a high operative risk [2, 5]. Therefore, as in this case, a conventional surgery should be preferred when operative Non-typhoidal Salmonella aortitis is a serious infection that risks are not prohibitive. Homograft should be the graft of carries a poor prognosis if unrecognized and not promptly choice, whenever it is available because of its highest resist- treated. It is mandatory to perform tests to search for extra- ance against reinfection [13]. intestinal infective localizations in patients with Salmonella Evidence from the literature suggests that surgery should spp. bacteremia, especially if the clinical and/or labora- be performed as soon as possible. On the other hand, the tory picture shows slow improvement during appropriate best timing depends on the clinical context. If the patient is antibiotic therapy or rapid worsening after interruption of hemodynamically stable with good fever and pain control, antibiotics. slow reduction of infammation indices and no signs of aor- In case of Salmonella spp. aortitis, predisposing condi- tic rupture, surgery can be delayed as long as a month from tions for bacteremia and vascular localization should be the clinical onset, never interrupting intravenous antibiotic checked (see Table 1).

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Table 1 Predisposing factors for cardiovascular localization by Sal- nontyphoidal salmonella bacteremia. Case Rep Med. 2018. https​ monella spp. [1–5, 7–10] ://doi.org/10.1155/2018/68456​17. 2. Strahm C, Lederer H, Schwarz EI, Bachli EB. Salmonella aortitis Male gender treated with endovascular aortic repair: a case report. J Med Case Age over 50 years Rep. 2012;6(1):1. https​://doi.org/10.1186/1752-1947-6-243. 3. Molacek J, Treska V, Baxa J, Certik B, Houdek K. Acute condi- Hypertension tions caused by infectious aortitis. Aorta. 2014;2(3):93–9. https​ Diabetes ://doi.org/10.12945​/j.aorta​.2014.14-004. Pathological alterations of the aortic wall (e.g. atherosclerosis) 4. Parekh PJ, Shams R, Challapallisri V, Marik PE. Successful treat- Invasive catheterization or post-traumatic lesions ment of Salmonella aortitis with endovascular aortic repair and antibiotic therapy. BMJ Case Rep. 2014. https​://doi.org/10.1136/ Immunodefciency (e.g. HIV infection) bcr-2014-20452​5. Solid-organ cancer 5. Guo Y, Bai Y, Yang C, Wang P, Gu L. Mycotic aneurysm due Atrial fbrillation to Salmonella species: clinical experiences and review of the Hemoglobinopathies literature. Braz J Med Biol Res. 2018;51(9):1–9. https​://doi. org/10.1590/1414-431X2​01868​64. Abnormal gastrointestinal barrier 6. Kommaraju K, Brinster DR. Endovascular abdominal aortic stent Intestinal strongyloidiasis grafting in unrecognized salmonella aortitis. Vasc Endovasc Surg. 2012;46(5):431–4. https​://doi.org/10.1177/15385​74412​44939​3. 7. Nakayama M, Fuse K, Sato M, et al. Infectious aortitis caused If possible, surgical treatment should always be per- by Salmonella Dublin followed by aneurysmal dilatation of the formed together with antibiotic therapy, to reduce mortal- abdominal aorta. Intern Med. 2012;51(20):2909–11. https​://doi. org/10.2169/inter​nalme​dicin​e.51.7937. ity. The best timing for surgical intervention depends on the 8. Montrivade S, Kittayarak C, Suwanpimolkul G, Chattranukulchai patient’s clinical status. Antibiotic therapy should be con- P. Emphysematous Salmonella aortitis with mycotic aneurysm. tinued for at least 6–8 weeks, considering long-life therapy BMJ Case Rep. 2017. https​://doi.org/10.1136/bcr-2017-22052​0. mostly in case of contraindications to conventional surgical 9. Kub CT, Kub TCT, Diseases I, Act R. Salmonella aortitis—a case of mistaken identity. ANZ J Surg. 2010;80(4):284–5. https​://doi. intervention or in case of performed endovascular procedure. org/10.1111/j.1445-2197.2010.05245​.x. Patients who have had aortic infection by Salmonella spp. 10. Looi JL, Cheung L, Lee APW. Salmonella mycotic aneurysm: have to be followed with clinical, blood, and radiological a rare cause of fever and back pain in elderly. Int J Cardiovasc examinations (angio-CT or angio-MRI) for years to be able Imaging. 2013;29(3):529–31. https​://doi.org/10.1007/s1055​ 4-012-0115-4. to act rapidly in case of complications or relapses after anti- 11. Erbel R, Aboyans V, Boileau C, et al. 2014 ESC guide- biotic suspension. lines on the diagnosis and treatment of aortic diseases. Russ J Cardiol. 2015;123(7):7–72. https​://doi.org/10.15829​ Acknowledgements We thank the participants who contributed to this /1560-4071-2015-07-7-72. report. 12. Luo C, Ko W, Kan C, Lin P, Yang J. In situ reconstruction of septic aortic pseudoaneurysm due to Salmonella or Streptococcus micro- Funding No funding was received. bial aortitis: long-term follow-up. J Vasc Surg. 2003;38:975–82. https​://doi.org/10.1016/s0741​-5214(03)00549​-4. 13. Mangioni D, Bonera G, Bonardelli S, Castelli F, Stellini R. Compliance with ethical standards Abdominal aortitis and aneurysm impending rupture during pneu- mococcal meningitis. Lancet Infect Dis. 2016;16(8):980. https​:// Conflict of interest The authors have no conficts of interest to declare. doi.org/10.1016/S1473​-3099(16)30114​-1.

Informed consent A consent for the use of the clinical data was pro- vided.

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